Adaptive evolution of rhizobial symbiotic compatibility mediated by co-evolved insertion sequences

Abstract

Mutualism between bacteria and eukaryotes has essential roles in the history of life, but the evolution of their compatibility is poorly understood. Here we show that different Sinorhizobium strains can form either nitrogen-fixing nodules or uninfected pseudonodules on certain cultivated soybeans, while being all effective microsymbionts of some wild soybeans. However, a few well-infected nodules can be found on a commercial soybean using inocula containing a mixed pool of Tn5 insertion mutants derived from an incompatible strain. Reverse genetics and genome sequencing of compatible mutants demonstrated that inactivation of T3SS (type three secretion system) accounted for this phenotypic change. These mutations in the T3SS gene cluster were dominated by parallel transpositions of insertion sequences (ISs) other than the introduced Tn5. This genetic and phenotypic change can also be achieved in an experimental evolution scenario on a laboratory time scale using incompatible wild-type strains as inocula. The ISs acting in the adaptive evolution of Sinorhizobium strains exhibit broader phyletic and replicon distributions than other ISs, and prefer target sequences of low GC% content, a characteristic feature of symbiosis plasmid where T3SS genes are located. These findings suggest an important role of co-evolved ISs in the adaptive evolution of rhizobial compatibility.

Comparative Genomics Reveals Broad Genetic Diversity, Extensive Recombination and Nascent Ecological Adaptation in Micrococcus luteus

“…On average, 94.6% of which could be annotated and functionally categorized using the eggNOG database [43]. ISFinder analysis [44] revealed a large number of insertion sequence (IS) elements in the genomes (7.22%~13.4% of the predicted CDSs, mean 8.51%), indicating strains in this species had undergone frequent genomic exchanges, and had a high genomic plasticity to adapt to the various environments [45,46]. There was also a weak correlation between genome size and the number of ISs among M. luteus strains (r = 0.31, p = 0.01).…”

Experimental Evolution of Legume Symbionts: What Have We Learnt?

“…On the other hand, some bacterial functions can be deleterious for symbiosis. For example, type 3 secretion systems (T3SS) were shown to decrease the symbiotic capacity of some rhizobium strains or prevent their interaction with some host plants [41,[45][46][47]. Furthermore, transfers of symbiotic genes performed under laboratory conditions did not always turn a non-symbiotic organism into an efficient legume symbiont.…”

NopD of Bradyrhizobium sp. XS1150 Possesses SUMO Protease Activity

“…However, besides secretion and translocation into host cells, only a few rhizobial T3 effectors have been biochemically characterized in detail. Examples of well-studied rhizobial effectors are the nodulation outer proteins NopE1/NopE2 (Wenzel et al, 2010;Schirrmeister et al, 2011), NopL (Bartsev et al, 2003;Bartsev et al, 2004;Zhang et al, 2011;Ge et al, 2016), NopM (Rodrigues et al, 2007;Kambara et al, 2009;Xin et al, 2012;Xu et al, 2018), NopP (Ausmees et al, 2004;Skorpil et al, 2005;Zhao et al, 2018;Sugawara et al, 2018), NopT (Dai et al, 2008;Dowen et al, 2009;Kambara et al, 2009;Fotiadis et al, 2012), and ErnA (Teulet et al, 2019).…”